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Immune Disorders and Its Correlation with Gut Microbiome http://dx.doi.org/10.4110/in.2012.12.4.129 RIEVIEW ARTICLE pISSN 1598-2629 eISSN 2092-6685 Immune Disorders and Its Correlation with Gut Microbiome † † Ji-Sun Hwang1 , Chang-Rok Im2 and Sin-Hyeog Im1* 1School of Life Sciences and Immune Synapse Research Center, Gwangju Institute of Science and Technology (GIST), Gwangju 500-712, 2Global Leader Program, Bugil Academy, Cheonan 330-941, Korea Allergic disorders such as atopic dermatitis and asthma are also exert beneficial effects by directly modulating immune common hyper-immune disorders in industrialized countries. system. For example, an oral treatment of certain probiotics Along with genetic association, environmental factors and or a mixture of them prevented and improved symptoms of gut microbiota have been suggested as major triggering fac- experimental inflammatory bowel disease, atopic dermatitis tors for the development of atopic dermatitis. Numerous and asthma by down-regulating inflammatory cytokines or in- studies support the association of hygiene hypothesis in al- ducing immune regulatory mechanisms. However, these ben- lergic immune disorders that a lack of early childhood ex- eficial effects are strain-specific (2-4), suggesting the necessity posure to diverse microorganism increases susceptibility to of development of screening system to identify specific pro- allergic diseases. Among the symbiotic microorganisms (e.g. gut flora or probiotics), probiotics confer health benefits biotics to treat specific disorders. through multiple action mechanisms including modification of Atopic dermatitis (AD) is chronic, relapsing inflammatory immune response in gut associated lymphoid tissue (GALT). skin disorder and a complex immune response mediated by Although many human clinical trials and mouse studies dem- genetic, environment factors and skin barrier dysfunction. onstrated the beneficial effects of probiotics in diverse im- Recently, the incidence of atopic dermatitis has remarkably mune disorders, this effect is strain specific and needs to ap- increased especially in the industrial cities compared to rural ply specific probiotics for specific allergic diseases. Herein, areas and developing countries, which strongly support the we briefly review the diverse functions and regulation mecha- “hygiene hypothesis” in the development of allergic immune nisms of probiotics in diverse disorders. disorders (5,6). Hygiene hypothesis has received worldwide at- [Immune Network 2012;12(4):129-138] tention from many scientists as the subject remains questioned for many years. Hygiene hypothesis states that a lack of early INTRODUCTION childhood exposure to infectious agents, symbiotic micro- organisms (e.g. gut flora or probiotics), and parasites increases “Probiotics” are defined as live microorganisms that, when susceptibility to allergic diseases by suppressing natural devel- administered in adequate amounts, confer a health benefit on opment of the immune system (7). Even though treatment the host (1). Although the beneficial effect of probiotics ad- with corticosteroid is the most well used method to treat atop- ministration was mainly known to improve the balance of in- ic dermatitis, long term usage of steroid can cause many side testinal microflora, recent studies showed that probiotics can effects including the atrophoderma and growth retardation Received on July 7, 2012. Revised on July 19, 2012. Accepted on July 27, 2012. CC This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribu- tion, and reproduction in any medium, provided the original work is properly cited. *Corresponding Author. Tel: 82-62-715-2503; Fax: 82-62-715-2484; E-mail: [email protected] †These authors contributed equally to this work. Keywords: Hygiene hypothesis, Intestinal microflora, Gut-Associated lymphoid tissue, Probiotics, Atopic dermatitis Abbreviations: GALT, Gut-Associated Lymphoid Tissue; GI, Gastrointestinal; MLN, Messenteric Lymph Node; AD, Atopic Dermatitis; HMP, Human Microbiome Project; IBD, Inflammatory Bowel Disease; T1D, Type 1 Diabetes; DC, Dendritic Cell; NOD, Nucleotide-binding Oligomerization Domain; TLT, Toll-Like Rceptor; Treg, Regulatory T Cells; iDO, Indoleamine 2,3-dioxygenase; SCORD, SCORing Atopic Dermatitis IMMUNE NETWORK www.immunenetwork.org Volume 12 Number 4 August 2012 129 Immune Disorders and Its Correlation with Gut Microbiome Ji-Sun Hwang, et al. (8). So many studies were focused on the development of ities and forty people inhibiting in cities by metagenomic innovative prevention and treatment strategies for AD to re- analysis, scientists discovered that the distribution of intestinal place the steroid treatment. Interestingly, recent studies also bacteria of the two groups has a stark contrast. Surprisingly, suggest the association of dysregulation of gut microbiota it was found that those living in rural habitats have about with diverse diseases including atopic dermatitis (9). There- three to five times more Lactobacillus acidophilus (LA). LA fore manipulation of the intestinal flora with good probiotics metabolizes lactic acid, obtains vitamin K, a cofactor for will be complementary and alternative treatments to divert blood clotting and healthy bone tissue turnover. LA also helps immune response from the hyper-immune states. In this re- recycle the amino acids in bile, and normalizes the body’s view, we summarized the hygiene hypothesis and its correla- cholesterol level compared to people living in cities. Possible tion with gut microbiome, especially on the aspect of pro- explanations to this phenomenon are attributing to the level biotics, in the development and regulation mechanisms of di- of stress and the difference in abiotic factors such as air and verse disorders. water and life span or health of people. Most importantly, distribution of helpful microorganisms is mainly derived from Microbiome and its relevance to the susceptibility of the types of foods consumed (19,20). The potential roles of diverse diseases microbiome on diverse disorders are summarized below. Several hypotheses have been proposed as the cause of de- Atopic dermatitis: Studies investigating the composition velopment in allergic disease, including atopic dermatitis. of the intestinal microflora in humans have shown the pivotal Among them, “hygiene hypothesis” has gained the most atten- role of commensal bacteria in the development of allergies. tions (7). This hypothesis explains that early childhood infection Studies comparing the microflora composition of atopic and caused by unhygienic contact with older siblings could prevent non-atopic infants also show significant differences. Non- the development of allergic disease (10). Later, Th1/Th2 para- atopic infants have more colonization of Bifidobacteria and digm was added that a lack of early childhood infection re- Lactobacillus in the intestine while there is much colonization sults a decreased Th1 immune response, which disturbs the of Clostridia in the intestine of atopic infants. However sev- Th1/Th2 balance and leads to an abundant Th2 response, eral reports also suggest that there are no significant differ- causing allergic disease (11). Later this hypothesis was further ences between the two groups (21,22). The exact role of in- revised, which considers changes in the intestinal colonization testinal flora in the development of atopic disease in the pattern during infancy and overlay hygienic lifestyle as the childhood is still not clarified (23). In addition to these quan- most important reasons for the increased allergy prevalence. titative differences in the Bifidobacterium, qualitative differ- Especially overlay hygiene can induce a lack of activity of ences have also been observed. The Bifidobacteria from atop- regulatory T cells, causing over-activation of Th1 as well as ic infants were found to induce much higher levels of pro-in- Th2 responses as the underlying mechanism of allergic disease flammatory cytokines in vitro whereas the Bifidobacteria from (12,13). non-atopic infants induced more secretion of anti-inflamma- As explained by hygiene hypothesis, a person’s life span tory cytokines. In addition to different secretion ability, differ- is largely affected by the distribution of intestinal bacteria. ential adhesion to intestinal mucosa may also result in a dif- The term “microbiome” was coined by Joshua Lederberg, ferent or reduced stimulation of the immune system through who argued that microorganisms inhabiting the human body the gut-associated lymphoid tissue (GALT) (24). should be included as part of the human genome, because Obesity: Obesity is associated with the changes in the rel- of their influence on human physiology and the human body ative abundance of the two dominant bacterial divisions, the contains over 10 times more microbial cells than human cells Bacteroids and the Firmicutes. The relative proportion of (14,15). To understand the microbiome (totality of microbes) Bacteroids is decreased in obese people compared to lean and the factors that influence the distribution and evolution people while the proportion of Firmicutes is increased in of the constituent microorganisms, the Human Microbiome obese people. Obese microbiome has an increased capacity Project (HMP) was initiated. HMP has aimed to identify and to harvest energy from the diet and colonization of germ-free characterize the microorganisms which are found in associa-
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